Multisensory pollution: Artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major)
Graphical abstract
Introduction
Urbanisation is one of the most important global changes and widely recognized as a primary source of modification of the natural environment (Vitousek et al., 1997; Rees and Wackernagel, 2008; Grimmet al., 2008). More people are now living in urban than rural areas (United Nations Population, 2018), and as this figure is projected to increase steadily over the next few decades, this will likely result in progressing urbanisation in most areas of the world, and particularly in developing countries (Seto et al., 2012). Urbanisation poses novel challenges to wild species as organisms are exposed to a suite of environmental factors that are either completely absent or of minor importance in rural and natural areas. Consequently, many studies have revealed profound phenotypic shifts in urban vs rural populations of the same species, which refer to many different traits and span different levels of biological organization (gene expression, hormone secretion, energy metabolism, behavioural traits) (Partecke, 2013; Albertiet al., 2017; Watson et al., 2017; Gill and Brumm, 2013; Magle et al., 2012).
In the last two decades, research in the field of adaptation to human activities has sought to identify the environmental drivers of such phenotypic shifts, often focusing on disentangling the effects of a single specific anthropogenic factor from all the many others that co-occur in human-dominated landscapes such as cities. Such an approach has been deployed in many correlative studies (Da Silva et al., 2014; Salmón et al., 2018; Murray et al., 2015; Francis et al., 2009; Raap et al., 2017a; Caorsi et al., 2019). Moreover, experimental work is also emerging, with many studies conducted in the field (Demeyrier et al., 2017; Morris-Drake et al., 2016; Spoelstraet al., 2017; Halfwerk and Slabbekoorn, 2009; Casasoleet al., 2017) but also in captivity (Dominoni et al., 2013a; Dorado-Correa et al., 2018). However, urban-specific environmental factors often co-occur and co-vary (Shepherd et al., 2016), and it is therefore crucial to study their combined impacts, particularly in cases where such combined impacts differs from the expected impacts based on estimated additive effects (McDonnell and Hahs, 2008; Halfwerk and Slabbekoorn, 2015). This is particularly relevant in cases where multiple environmental stressors influence similar phenotypic traits. Combined effects may be additive (whole being equal to the exact sum of parts), antagonistic (whole being lesser than the sum of parts), or synergistic (whole being greater than the sum of parts) (Chanet al., 2010; Hale et al., 2017; McMahon et al., 2017).
Artificial light at night and anthropogenic noise have recently received increasing attention, with studies focusing on the impact of these so-called sensory pollutants on phenotypic traits related to an animal’s perception, physiology and behaviour (Halfwerk and Slabbekoorn, 2015; Swaddleet al., 2015; Shannon, 2016; Gaston et al., 2017; Spoelstraet al., 2015). The impact of both sensory pollutants has been linked to changes in survival and reproductive performance across a wide range of taxa, including birds (Habib et al., 2007; Halfwerk et al., 2011), mammals (Bunkley et al., 2015), fish (Simpsonet al., 2016; Nedelecet al., 2016) and insects (Lampe et al., 2012). Experimental studies have revealed how noise and light pollution influence perceptual processes during foraging (Siemers and Schaub, 2011), mating (Kempenaers et al., 2010; Halfwerket al., 2011) or predator avoidance (Morris-Drake et al., 2017; Meillère et al., 2015). Furthermore, many studies have assessed how animals cope with these perceptual impacts by adjusting their behaviour (Halfwerk et al., 2012; de Jong et al., 2016; Ware et al., 2015) and physiology (Blickley et al., 2012), and in few cases their perceptual sensitivities (Gomeset al., 2016; Danilovichet al., 2015). The impacts of light and noise on the activity patterns of birds have been particularly well studied. Correlating levels of artificial night lighting to onset of dawn song has repeatedly revealed that song birds in light-polluted areas start their dawn song earlier (Da Silva et al., 2014; Dominoni and Partecke, 2015; Miller, 2006), and that the effect of light-pollution varies with the season (Da Silva et al., 2015; Raap et al., 2017b), as well as with species-specific sensitivities to light (Kempenaers et al., 2010; Sun et al., 2017). Experimental exposure in the lab confirmed a causal link between light levels at night and nocturnal and crepuscular activity in several bird species (Dominoni et al., 2013b; Dominoniet al., 2018; de Jonget al., 2016; de Jong et al., 2017). A recent field experiment, however, has failed to indicate that light pollution can affect onset of dawn song in several bird species (Da Silvaet al., 2017), although the illumination might have been too localized to have an impact as birds could easily roost in nearby dark locations (de Jong et al., 2016). Studies on anthropogenic noise, in particular generated by traffic, have revealed that birds start singing in earlier, or may even switch to singing at night in noisier territories (Dominoni et al., 2016; Fuller et al., 2007). Experimental exposure in the field confirmed a causal link between noise levels around sunrise and the onset of dawn singing of a community of bird species (Arroyo-Solís et al., 2013).
Despite the fact that light at night and noise often co-occur, in particular in urbanised areas (Votsi et al., 2017), few studies so far have addressed how these two sensory pollutants can influence each other’s impact. In birds, several correlational studies investigated the combined effects of light and noise on activity patterns, with contrasting results. In European robins (Erithacus rubecola), daytime noise rather than light at night has been suggested to drive nocturnal singing behaviour (Fuller et al., 2007). Later studies contradicted this result in robins and also in other songbirds species, suggesting that light was the strongest predictor of nocturnal activity (Da Silva et al., 2014; Fuller et al., 2007; Nordt and Klenke, 2013; Dominoni et al., 2014). The experimental studies conducted in the field were usually designed to manipulate either one or the other variable, but not both simultaneously (Casasoleet al., 2017). Moreover, in several cases the levels of the non-manipulated variable was not even measured, thus failing to control for small scale variation in light and noise levels that may have affected the interpretation of the results (Da Silvaet al., 2017; Arroyo-Solís et al., 2013; Raap et al., 2015). In general, all these studies typically ignored testing for potential interaction effects between the two sensory pollutants. The few studies that used a full-factorial experimental exposure to noise and light pollution either yielded inconclusive results or did not specifically test whether the combined impact is additive, antagonistic or synergistic (Hale et al., 2017; McMahon et al., 2017; Chan et al., 2010).
Here we aim to combine knowledge and insights from studies on both light and noise pollution to address whether these two sensory stimuli can influence each other’s impact. Specifically, we asked whether the combined impact of noise and light was additive, synergistic or antagonistic (Fig. 1). We collected male great tits (Parus major) from both urban and rural areas and kept these birds in the lab under controlled noise and light levels. We used birds from different populations to specifically test whether urban birds might have developed a different sensitivity/tolerance to light at night and noise, as previous studies suggested this might be the case (Davies et al., 2017). We exposed each individual to moderate levels of anthropogenic noise and artificial light at night using a balanced, full-factorial, repeated measures design. We automatically scored an animal’s activity level by recording the number of perch hops individuals performed in their experimental cage and used this data to calculate their activity during various parts of the day and night, as well as the onset and offset of their daily cycle.
Section snippets
Experimental subjects
The experiment was carried out at the Netherlands Institute of Ecology (NIOO-KNAW) in Wageningen, The Netherlands between 19th of February and March 17, 2018. Male great tits were caught in September 2017 in several rural (17 birds) and urban areas (16 birds) throughout the Netherlands (see Suppl. Table 1 for details on sampling locations). Birds were individually housed in cages (90 × 50 × 40cm) prior to and during the experiment. During the experiment, the front side of the cages was covered
Treatment effects on amount of activity
We found a significant three-way interaction effect of light, noise and origin on the total activity (χ2 = 17.9, p < 0.001, suppl. Table 1). We then split the dataset between urban and forest birds and found for both populations a significant light*noise interaction (urban: χ2 = 32.5, p < 0.001; forest: χ2 = 5.2, p = 0.023; suppl. Table 1). Light alone had a significant effect on total activity of both urban and forest birds, increasing it by 24 min in urban birds and 12 min in forest birds
Discussion
Understanding how human activity shapes activity of wild animals is a global research challenge (Gaynor et al., 2018). In recent years, the impact of artificial light at night and anthropogenic noise have received much attention. However, there is considerable debate about the relative importance of each of these stimuli in affecting activity of wildlife, mostly due to a lack of experimental work. Here we show, via an experimental manipulation, that both light and noise can affect activity
Conclusions
We have shown that artificial light at night and noise interact and produce complex effects on activity patterns of a model songbird species. On the one hand, light at night may override a daytime effect of noise, whereas on the other hand, continuous noise exposure may enhance the effect of light during the night as well as around dusk and dawn, more than the simple addition of the single effects of these stimuli. Thus, our results point to multisensory pollution being a considerable threat to
Author contributions
DMD, JAHS, MEV, WH conceived the study and designed the experiment. DMD caught the birds in the wild. JAHS with the help of DMD and WH performed the experiment. JAHS analysed the data with input from DMD and WH. DMD wrote the paper with help from all co-authors. All authors agreed on the final version of the manuscript.
Declaration of competing interest
We declare no conflicting interests.
Acknowledgements
We wish to thank all the people who helped us catching birds in the field: Robin Heinen, Martijn van der Sluijs and Peter Alblas. We are also grateful to Coretta Jongeling, Ruben de Wit, Franca Kropman and Marylou Aaldering for providing outstanding care to all the birds in this experiment. Jeroen Laurens provided technical assistance for the installation of the light and noise systems and the activity recorders. Zeynep Ulgezen and Teemu Kapyla also provided immense help in setting up the
References (86)
- et al.
Anthropogenic noise alters bat activity levels and echolocation calls
Glob. Ecol. Conserv.
(2015) Neither artificial light at night, anthropogenic noise nor distance from roads are associated with oxidative status of nestlings in an urban population of songbirds
Comp. Biochem. Physiol. Part A Mol. Integr. Physiol.
(2017)Increased amplitude and duration of acoustic stimuli enhance distraction
Anim. Behav.
(2010)Bats regulate biosonar based on the availability of visual information
Curr. Biol.
(2015)- et al.
Noise pollution changes avian communities and species interactions
Curr. Biol.
(2009) - et al.
A behavioural mechanism explaining noise-dependent frequency use in urban birdsong
Anim. Behav.
(2009) Dose-dependent responses of avian daily rhythms to artificial light at night
Physiol. Behav.
(2016)- et al.
Artificial night lighting affects dawn song, extra-pair siring success, and lay date in songbirds
Curr. Biol.
(2010) - et al.
Urban wildlife research: past, present, and future
Biol. Conserv.
(2012) - et al.
Cross-modal impacts of anthropogenic noise on information use
Curr. Biol.
(2016)